Helminth’s assemblage of Trachemys dorbigni (Testudines: Emydidae) in southern Brazil: implications of anthropogenic environments and host’s genders

Assembleia de helmintos de Trachemys dorbigni (Testudines: Emydidae) no sul do Brasil: implicações dos ambientes antrópicos e do gênero sexual dos hospedeiros

ABSTRACT

The assemblage of helminths of Trachemys dorbigni was analyzed according two environments (rural and urban) and according to host’s gender. Thus, the helminths found were: Spiroxys contortus (Rudolphi, 1819), Falcaustra affinis (Leidy, 1856), Camallanus emydidius Mascarenhas & Müller, 2017, Dioctophyme renale (Goeze, 1782) (larvae), Eustrongylides sp. (larvae) (Nematoda), Telorchis corti (Stunkard, 1915), Telorchis achavali Mañé-Garzón & Holcman-Spector, 1973, Telorchis spp. (Digenea), Polystomoides rohdei Mañé-Garzón & Holcman-Spector,1968 and Neopolystoma sp. (Monogenoidea). Parasitological indices suggests that S. contortus, F. affinis, C. emydidius, T. corti and P. rohdei are species common in helminth assemblage of T. dorbigni in southern Brazil. Infection by Dioctophyme renale is typical of the urban area and suggest relation with eutrophication process and feedback of parasitic cycle in the freshwater urban environment. Parasitological indices of Neopolystoma sp. and T. achavali suggest to be occasional infections; whereas infection by Eustrongylides sp. could be considered accidental. About Telorchiidae, there was no co-occurrence of the species of this group for the examined hosts. In relation to host’s gender, it was observed that infections by S. contortus, F. affinis, C. emydidius and T. corti had higher rates in females, showing a more intimate association with the females of T. dorbigni. The results suggest that human impact on the environment could affect the infrapopulacional dynamics of parasite species influencing the presence and rates of infection of helminths or exacerbating heterogeneities related to host’s gender.

KEYWORDS
Freshwater turtles; D’Orbigny’s slider turtle; parasites; rural area; urban area

RESUMO

A assembleia de helmintos de Trachemys dorbigni foi analizada de acordo com dois ambientes (rural e urbano) e de acordo com o gênero sexual dos hospedeiros. Os helmintos encontrados foram: Spiroxys contortus (Rudolphi, 1819), Falcaustra affinis (Leidy, 1856), Camallanus emydidius Mascarenhas & Müller, 2017, Dioctophyme renale (Goeze, 1782) (larva), Eustrongylides sp. (larva) (Nematoda), Telorchis corti (Stunkard, 1915), Telorchis achavali Mañé-Garzón & Holcman-Spector, 1973, Telorchis spp. (Digenea), Polystomoides rohdei Mañé-Garzón & Holcman-Spector,1968 and Neopolystoma sp. (Monogenoidea). Os indices parasitológicos sugerem que S. contortus, F. affinis, C. emydidius, T. corti e P. rohdei são espécies comuns da assembleia de helmintos de T. dorbigni no extremo sul do Brasil. A infecção por Dioctophyme renale é tipica da area urbana e sugere estar relacionada com os processos de eutrofização e a retroalimentação do ciclo parasitário no ambiente aquático urbano. Os indices parasitológicos de Neopolystoma sp. e T. achavali sugerem que a infecção por estes seja occasional; a infecção por Eustrongylides sp. pode ser considerada acidental. Não houve co-ocorrência entre as espécies de Telorchiidae. Em relação ao gênero sexual, observou-se que as infecções por S. contortus, F. affinis, C. emydidius e T. corti apresentaram taxas mais elevadas nas fêmeas, mostrando uma associação mais íntima com as fêmeas de T. dorbigni. Os resultados sugerem que o impacto humano sobre o ambiente pode afetar a dinâmica das infrapopulações dos helmintos parasitos, influenciando a presença e os índices de infecção de helmintos ou exacerbando heterogeneidades relacionadas ao gênero sexual dos hospedeiros.

PALAVRAS-CHAVE
Tartarugas dulceaquícolas; tigre d’água; parasitos; área rural; área urbana

Parasitism involves a homoplastic and historical condition in nearly every animal group (Bush et al., 2001; Dobson et al., 2008; Pizzi, 2009). This condition is ruled by selective processes of host-parasite coevolution (Combes, 1997; Dybdahl & Storfer, 2003). Several factors - that is, heterogeneities - of both host and parasite are important for parasite life cycles to be properly developed (Von Zuben, 1997; Wilson et al., 2002). For the host, these heterogeneities involve gender, sexual dimorphism, reproductive condition, habitat use during the reproductive process, age, diet, and geographical distribution (Von Zuben, 1997; Wilson et al., 2002; Klein, 2004). For parasites, these heterogeneities include size, quantity, fertility rate, reproduction mechanisms, and intra- or inter-host dispersion ability (Crofton, 1971; Von Zuben, 1997; Wilson et al., 2002; Khokhlova et al., 2010).

Concerning to Trachemys dorbigni (Duméril & Bibron, 1835) (Emydidae) helminths, there have been morphological studies including new species descriptions and host records, thus expanding knowledge on the geographical distribution of known species (Mañé-Garzón & Holcman-Spector, 1968a,b,1973; Mascarenhas & Müller, 2013, 2015a,b, 2017; Bernardon et al., 2014).

Trachemys dorbigni occurs in Brazil, Uruguay and Argentina (Rhodin et al., 2017). In Brazil, it is one of the most abundant freshwater turtles in Rio Grande do Sul State (Bujes et al., 2011); in addition, it can usually be found in heavily anthropogenic urban environments, such as sewage systems, as well as in rural environments, as rice crop water drainage channels with pesticide residues (Bujes & Verrastro, 2008; Fagundes et al., 2010).

Thus, the lack of knowledge on T. dorbigni helminths biodiversity in anthropic environments have justified the development of this study, which analyzes helminth’s assemblage of T. dorbigni in southern Brazil according to urban and rural environments and hostʼs gender.

MATERIALS AND METHODS

Sixty T. dorbigni were collected between July 2010 and December 2012 in two distinct areas, an urban and a rural, in the state of Rio Grande do Sul, Brazil. The sampling period encompassed spring and summer months in the southern hemisphere. Only two hosts were sampled in July 2010.

Twenty-eight freshwater turtles (13 males: 15 females) were collected in four ponds in the rural area from at the Centro Agropecuário da Palma from the Universidade Federal de Pelotas (UFPel) located in Capão do Leão county (31°48ʼ01.1ˮS - 52°30ʼ48.6ˮW) (Fig. 1A). Another 32 hosts (14 males: 18 females) were collected in channels in the urban area of the city of Pelotas (31°46ʼ16.9ˮS - 52°18ʼ45.9ˮW) (Fig. 1B). Average weigh and average linear carapace length of females and males was 1494.7 grams; 207.6 mm, and 825 grams; 175.7 mm, respectively. The sexing was done during necropsy with the examination of the reproductive system.

Fig. 1.
Overall layout of the collection environments in the study of helminth assemblage of Trachemys dorbigni in southern Brazil: A, detail of the Centro Agropecuário da Palma (UFPel), rural area of Capão do Leão, State of Rio Grande do Sul, Brazil; B, detail of the urban área of Pelotas, Rio Grande do Sul, Brazil. Source: extracted and modified the site Google^® Earth (©2014 Google - Images ©2014 Digital Globe).

The freshwater turtles were anesthetized with a combination of 10% ketamine and 2% xylazine; after analgesia, a 2% lidocaine hydrochloride intrathecal injection was administered, as recommended by Resolution 1000/2012 of the Conselho Federal de Medicina Veterinária (2012). This study was licensed by the Instituto Chico Mendes para Conservação da Biodiversidade (23196-ICMBio) and was approved by the Ethics and Animal Experimentation Committee of the Universidade Federal de Pelotas (3026 - CEEA/UFPel).

The nasal and oral cavity, eyes, carapace and plastron, nails, skin folds, skin-carapace and plastron-skin insertions were examined. At necropsy, the plastron was removed by osteotomy of its lateral processes and circumferential integument section for general observation and splanchnological screening. The viscera were isolated anatomically according to system, i.e. respiratory, digestive, reproductive and urinary systems. After that, the splanchnological systems were lacquered and divided into their anatomical and functional parts: esophagus and stomach together and separately, as well as the small and large intestines. The same procedure was applied to the other splanchnological systems, according to their anatomical and functional divisions. Host voucher specimens were deposited in the Coleção Herpetológica do Museu de Ciências Naturais Carlos Ritter (UFPel), Rio Grande do Sul, Brazil (numbers 78-79).

Helminths were fixed in AFA (70°GL ethanol, 37% formaldehyde, glacial acetic acid). Nematoda taxa were preserved in 70°GL glycerin ethanol and then mounted on semi-permanent slides with Amannʼs lactophenol. Digenea and Monogenoidea were preserved in 70°GL ethanol, stained with Langeronʼs carmine or Delafield hematoxylin, and assembled in Canada balsam (Amato et al., 1991). Helminths were identified based on morphological and morphometric characteristics according to Hedrick (1935), Mace & Anderson (1975), Measures & Anderson (1985), Baker (1986), Measures (1988), Moravec & Vargas-Vázquez (1998) and Mascarenhas & Müller (2017) to Nematoda; Mañé-Garzón & Holcman-Spector (1973) and MacDonald & Brooks (1989) to Digenea; Mañé-Garzón & Holcman-Spector (1968a) and Pichelin (1995) to Monogenoidea. Vouchers were deposited in Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC), Rio de Janeiro, Brazil; Coleção de Helmintos do Laboratório de Parasitologia de Animal Silvestres (CHLAPASIL-UFPel), Pelotas, Rio Grande do Sul State, Brazil, and Coleção de Invertebrados do Museu de La Plata (MLP), La Plata, Argentina (Tab. I).

Tab. I.
Helminths of Trachemys dorbigni (Duméril & Bibron, 1835) (Emidydae) (n=60) on the southern Brazil and their site of infection, parasitological indices (P%, Prevalence; MII, Mean Intensity of Infection; MA, Mean Abundance) and Range (RA) (CHIOC, Coleção Helmintológica do Instituto Oswaldo Cruz; MLP, Coleção de Invertebrados do Museu de La Plata; CHLAPASIL, Coleção de Helmintos do Laboratório de Parasitologia de Animais Silvestres da Universidade Federal de Pelotas).

Helminths	Site of infection	P (%)	MII	MA	RA	Vouchers
NEMATODA
Spiroxys contortus	Heart; esophagus; stomach, small intestine; large intestine	68.33	70.17	47.95	1 - 1184	35875-35876 (CHIOC) 6740-6744 (MLP) 472-476 (CHLAPASIL)
Falcaustra affinis	Heart; stomach; large intestine; kidney	85	92.39	78.53	1 - 472	35873-35874 (CHIOC) 6745-6747 (MLP) 477-480 (CHLAPASIL)
Camallanus emydidius	Lung; stomach; small intestine; large intestine	100	30.31	30.31	1 - 242	38507-38512 (CHIOC) 523-527 (CHLAPASIL)
Dioctophyme renale (larva)	Coelomic cavity; muscles; stomach (serous); mesentery; surface of various organs: heart, lung, liver, pancreas, spleen and intestines	50	13.03	6.51	1 - 129	519-521 (CHLAPASIL)
Eustrongylides sp. (larva)	Stomach (serous)	1.66	1	0.016	1	522 (CHLAPASIL)
DIGENEA
Telorchis corti	Small intestine	36.66	25.36	9.3	1 - 130	37846-37850 (CHIOC) 6748-6749 (MLP) 481-504 (CHLAPASIL)
Telorchis achavali	Small intestine	1.66	3	0.05	3	505-507 (CHLAPASIL)
Telorchis spp.	Small intestine	10	2.16	0.21	1 - 6	516-517 (CHLAPASIL)
MONOGENOIDEA
Polystomoides rohdei	Oral cavity	81.66	16.81	13.73	1 - 132	530-544 (CHLAPASIL)
Neopolystoma sp.	Urinary bladder	1.66	2	0.03	2	528-529 (CHLAPASIL)

The T. dorbigni helminth assemblage was analyzed by Prevalence (P%), Mean Intensity of Infection (MII), Mean Abundance (MA) (Bush et al., 1997). Parasitological indices were calculated for all sampled hosts as well as for host gender (Male: M; Female: F) and environment (Rural: R; Urban: U). Thus, P% and MII were compared in four different ways: 1) between hosts from rural (RM + RF) and urban (UM + UF) environment; 2) between host’s genders (RM + UM) x (RF + UF); 3) between males and females from the same environment (RMxRF; UMxUF); and, 4) between individuals of the same gender from different environments (RMxUM; RFxUF). Prevalence indices were compared by using exact Fisher's test “F” (p≤0.05) and MII indices were compared by using Bootstrapʼs confidence interval (BC _α , p≤0.05) in Quantitative Parasitology (QP 3.0) software (Reiczigel et al., 2019).

RESULTS

Considering all sampled hosts: (RM+RF) + (UM+UF). All examined hosts (n = 60) were parasitized by helminths (Nematoda, Digenea, and Monogenoidea). The Nematoda found included Spiroxys contortus (Rudolphi, 1819) (Gnathostomatidae), Falcaustra affinis (Leidy, 1856) (Kathlaniidae), Camallanus emydidiusMascarenhas & Müller, 2017 (Camallanidae), Dioctophyme renale (Goeze, 1782), Eustrongylides sp. (Dioctophymatidae); Digenea consisted of Telorchis corti (Stunkard, 1915), Telorchis achavaliMañé-Garzón & Holcman-Spector, 1973 and Telorchis spp. (Telorchiidae), while Monogenoidea included Polystomoides rohdei Mañé-Garzón & Holcman-Spector,1968 and Neopolystoma sp. (Polystomatidae).

Dioctophyme renale and Eustrongylides sp. occurred only as third-stage larvae (one larva per cyst) (Tab. I). Telorchis spp. were represented by immature specimens. There were no co-infections between T. achavali, T. corti and immature Telorchis spp., that is, Telorchiidae species occurred in different hosts. Eustrongylides sp., T. achavali and Neopolystoma sp. infections showed low parasitic indices, suggesting that these infections are occasional or incidental for this host. Helminths found and their respective infection sites, prevalence, mean intensity of infection, and mean abundance are shown in Tab. I.

Comparison of the helminth assemblage of T. dorbigni in relation to environment: (RM + RF) x (UM + UF). Table II shows the parasitological indices of helminths by comparing rural and urban environments. The results showed a species-specific fluctuation of these indices between the two studied environments. Among the Nematoda species found, only two showed statistical differences for prevalence. Spiroxys contortus presented a higher prevalence (85.7%) in the countryside, differing from urban area (53.1%), whereas D. renale showed higher prevalence (87.5%) in the urban environment as opposed to rural area (7.1%). As to mean intensity of infection, only C. emydidius showed differences between rural and urban areas, with 16.46 and 42.44 helminths/host, respectively. Among the Nematoda species, C. emydidius was the most prevalent (100%) in both environments.

Tab. II.
Prevalence (P%), Mean Intensity of Infection (MII) and Mean Abundance (MA) and Range (RA) of helminths of Trachemys dorbigni (Duméril & Bibron, 1835) (Emidydae) (n=60) from rural and urban environments on the southern Brazil [n, number of sampled hosts; a, b, differences between the environments (exact Fisher's test “F”, p≤0.05, for P% and Bootstrapʼs confidence interval, p≤0.05, for MII)].

Helminths	Environments
	Rural (n=28)				Urban (n=32)
	P%	MII	MA	RA	P%	MII	MA	RA
NEMATODA
Spiroxys contortus	85.7a	112.58	96.5	6 - 1184	53.1b	10.29	5.46	1 - 41
Falcaustra affinis	85.7	85.42	73.21	1 - 305	84.4	98.59	83.18	2 - 472
Camallanus emydidius	100	16.46a	16.46	1 - 54	100	42.44b	42.44	1 - 242
Dioctophyme renale (larva)	7.1a	1.5	0,1	1 - 2	87.5b	13.86	12.12	1 - 129
Eustrongylides sp. (larva)	-	-	0	-	3.1	1	0.03	1
DIGENEA
Telorchis corti	3.6a	130	4.64	130	65.6b	20.38	13.37	1 - 120
T. achavali	3.6	3	0.1	3	-	-	0	-
Telorchis spp.	21.4	2.16	0.46	1 - 6	-	-	0	-
MONOGENOIDEA
Polystomoides rohdei	100a	19.93	19.93	1 - 132	65.6b	12.67	8.31	1 - 46
Neopolystoma sp.	-	-	0	-	3.1	2	0.06	2

Considering Digenea, T. corti was the only species that occurred in both rural and urban areas. This species only showed prevalence differences between the environments studied, which were higher in urban area hosts (65.6%) in contrast to rural area, which were 3.6%. Monogenoidea species, P. rohdei, showed an occurrence pattern similar to that of T. corti, occurring in both environments. However, this species was more prevalent in rural area (100%) than for urban area (65.6%). Mean abundance and range basically reinforce the differences observed for S. contortus, C. emydidius, D. renale, T. corti and P. rohdei. Prevalence differences occurred in species of parasites with greater mean abundance and range fluctuations between environments. Mean abundance and range of S. contortus showed that the parasitic loads were higher in the rural environment. Dioctophyme renale and C. emydidius showed mean abundance and range with expressive values in the freshwater turtles from urban environment. Among species occurring in both urban and rural areas, only F. affinis showed no prevalence or mean intensity of infection differences between the two areas. Telorchis achavali and Telorchis spp. occurred only in rural hosts. On the other hand, Eustrongylides sp. and Neopolystoma sp. were present only in urban hosts (Tab. II). Low prevalence and mean intensity of infection values for Eustrongylides sp., T. achavali and Neopolystoma sp. for each environment as well as for the whole sample reinforced the hypothesis that these infections in T. dorbigni may be accidental or occasional.

Comparing helminth assemblage of T. dorbigni between host’s gender independently of sampled environments: (RM + UM) x (RF + UF). On comparing helminth assemblage of male and female, it was observed that infection by F. affinis, S. contortus, and T. corti was more prevalent in female hosts, with values of 93.9%, 81.8%, and 48.5%, respectively. Likewise, C. emydidius mean intensity of infection was significantly higher in female hosts (42.12 helminths/host). Another observation made was that only T. dorbigni females showed infection by Eutrongylides sp., T. achavali and Neopolystoma sp., with each species occurring isolatedly in a different female host, with extremely low parasitological indices (Tab. III). The other parasites occurred in both genders of the T. dorbigni.

Tab. III
Prevalence (P%), Mean Intensity of Infection (MII) and Mean Abundance (MA) and Range (RA) of helminths in males and females of Trachemys dorbigni (Duméril & Bibron, 1835) (Emidydae) (n=60) on the southern Brazil [n, number of sampled hosts; a, b, differences between the host’s gender (exact Fisher's test “F”, p≤0.05, for P% and Bootstrap´s confidence interval, p≤0.05, for MII)].

Helminths	Host’s gender
	Male (n=27)				Female (n=33)
	P%	MII	MA	RA	P%	MII	MA	RA
NEMATODA
Spiroxys contortus	51.9a	42.64	22.11	1 - 338	81.8b	84.44	69.09	1 - 1184
Falcaustra affinis	74.1a	62.1	46	2 - 472	93.9b	111.94	105.15	1 - 427
Camallanus emydidius	100	15.89a	15.89	1 - 73	100	42.12b	42.12	1 - 242
Dioctophyme renale (larva)	48.1	14	6.74	2 - 57	51.5	12.29	6.33	1 - 129
Eustrongylides sp. (larva)	-	-	0	0	3.03	1	0.03	1
DIGENEA
Telorchis corti	22.2a	16.83	3.74	1 - 59	48.5b	28.56	13.85	1 - 130
T. achavali	-	-	0	0	3.03	3	0.09	3
Telorchis spp.	7.4	1	0.07	1	12.1	2.75	0.33	1 - 6
MONOGENOIDEA
Polystomoides rohdei	74.1	13.15	9.74	1 - 79	87.9	19.34	17	1 - 132
Neopolystoma sp.	-	-	0	0	3.03	2	0.06	2

Comparing helminth assemblage of T. dorbigni between host’s genders from the same environment: RMxRF; UMxUF. With reference to prevalence of helminths of male and female hosts from the same environment, it was observed that infection by S. contortus and F. affinis was more prevalent in females (100% and 100%, respectively) than in males in rural area. This pattern was also observed to T. corti in urban area, where this species showed higher prevalence (83.3%) in females (Tab. IV). As to mean intensity of infection, there were differences between host’s genders for infection of C. emydidius in urban area, where female hosts showed significantly higher values for this Nematoda than males. These analyses reinforce the comparisons between helminth assemblage in the male and female hosts (RM + UM) x (RF + UF) listed above. For these helminths, the analyses seem to suggest the occurrence of a dominant-female host pattern.

Tab. IV.
Prevalence (P%), Mean Intensity of Infection (MII) and Mean Abundance (MA) and Range (RA) of helminths in males and females of Trachemys dorbigni (Duméril & Bibron, 1835) (n=60) (Emidydae) on the southern Brazil according to rural and urban environments [n, number of sample hosts; a, b, differences between the host’s gender of the same environments; ■,■■ differences for the same gender between site of study (exact Fisherʼs test “F”, p≤0.05, for P% and Bootstrapʼs confidence interval, p≤0.05, for MII)].

Helminths	Parasitological indices	Environments
		Rural		Urban
		Host’s gender		Host’s gender
		Male (n=13)	Female (n=15)	Male (n=14)	Female (n=18)
NEMATODA
Spiroxys contortus
	P%	69.2a	100b; ■	35.7	66.7■■
	MII	64.33	141.53	3.6	13.08
	MA	44.54	141.53	1.29	8.72
	RA	6 - 338	8 - 1184	1 - 7	1 - 41
Falcaustra affinis
	P%	69.2a	100b	78.6	88.9
	MII	50.33	106.47	71.73	117.06
	MA	34.85	106.47	56.36	104.06
	RA	4 - 191	1 - 305	2 - 472	8 - 427
Camallanus emydidius
	P%	100	100	100	100
	MII	13.92	18.67■	17.71a	61.67b;■■
	MA	13.92	18.67	17.71	61.67
	RA	3 - 44	1 - 54	1 - 73	1 - 242
Dioctophyme renale (larva)
	P%	-	13.3■	92.9	83.3■■
	MII	-	1.5	14	13.73
	MA	0	0.2	13	11.44
	RA	0	1 - 2	2 - 57	1 - 129
Eustrongylides sp. (larva)
	P%	-	-	-	5.6
	MII	-	-	-	1
	MA	0	0	0	0.06
	RA	0	0	0	1
DIGENEA
Telorchis corti
	P%	-	6.7■	42.9a	83.3b;■■
	MII	-	130	16.83	21.8
	MA	0	8.67	7.21	18.17
	RA	0	130	1 - 59	1 - 120
T. achavali
	P%	-	6.7	-	-
	MII	-	3	-	-
	MA	0	0.2	0	0
	RA	0	3	0	0
Telorchis spp.
	P%	15.54	26.7	-	-
	MII	1	2.75	-	-
	MA	0.15	0.73	0	0
	RA	1	1 - 6	0	0
MONOGENOIDEA
Polystomoides rohdei
	P%	100■	100	50■■	77.8
	MII	15.77	23.53	8.29	14.86
	MA	15.77	23.53	4.14	11.56
	RA	1 - 79	2 - 132	1 - 25	1 - 46
Neopolystoma sp.
	P%	-	-	-	5.6
	MII	-	-	-	2
	MA	0	0	0	0.11
	RA	0		0	2

Comparing helminth assemblage of T. dorbigni for the same host’s gender between environments: RMxUM; RFxUF. By comparing parasitological indices for parasites between males from rural and urban areas, prevalence differences were found only for P. rohdei, which was higher in rural area males (100%). As to female host infection in both rural and urban areas, differences in prevalence for S. contortus, D. renale and T. corti were found; females from rural area showed a higher prevalence for S. contortus (100%), whereas females from urban area presented higher prevalence for D. renale (83.3%) and T. corti (83.3%). Concerning to mean intensity of infection, differences between female hosts from the two environments were only observed for C. emydidius, which was higher in females from urban area (61.67 helminths/host). Other parasite species either did not differ or could not be analyzed due to restrictions related to host’s gender, as shown in previous analyses. With reference to host’s gender, T. achavali occurred in only one RF, while Eustrongylides sp. and Neopolystoma sp. occurred isolatedly in one UF. These helminths showed extremely low parasitological indices (Tab. IV), as previously mentioned.

DISCUSSION

Anthropic environmental implications on helminth assemblage of T. dorbigni. Windsor (1998) and Dobson et al. (2008) have argued that most of the worldʼs species are parasites, upon considering the relation between the number of parasite species and a single host species. This supremacy in the number of parasitic species can be explained by the plasticity of certain parasite groups, such as Nematoda, in the face of selection pressure of the environment. Jairajpuri (2005) discussed the plasticity of Nematoda considering the high irradiation of the group, and the consequent diversity, to different environments and life conditions. On considering T. dorbigni parasite groups and the two anthropic environments studied, parasitological indices relating to Nematoda (S. contortus, F. affinis and C. emydidius) reveal this (co-evolutionary) plasticity, which is typical of the group in the face of the environmental diversity which they may be exposed. Falcaustra affinis specifically showed high parasitological indices in both urban and rural environments, proving to be the most successful Nematoda for the host species in both environments. Falcaustra affinis success can be proved by its high infection as compared to other Nematoda found, such as S. contortus, C. emydidius and D. renale. Mean intensity of infection and mean abundance observations for S. contortus, C. emydidius and D. renale suggest that these parasites have not had the same infection success in the host species in both environments.

The same plasticity pattern between the two environments studied can be extended to Digenea and Monogenoidea. Digenea species that showed greatest plasticity was T. corti, while for Monogenoidea was P. rohdei. Thus, it can be said that parasite loads suggest that these species may be commonly found in the helminth assembly of T. dorbigni in the study area, regardless of the sampled environment.

On the other hand, considering parasitological indices of Eustrongylides sp., T. achavali and Neopolystoma sp., other interpretations can be suggested, such as an accidental infection by T. dorbigni. Parasitological indices are tools that demonstrate host-parasite fitness (Rósza et al., 2000; Reiczigel et al., 2005). This host-parasite evolutionary fitness constitutes a historical relationship and indices such as prevalence are commonly used to predict and estimate the parasite load or parasitic pressure on a particular host species (Gregory & Blackburn, 1991). In this context, the accidental infection hypothesis can be more easily understood in relation to Eustrongylides sp., since species of this genus occur in waterfowl (definitive hosts) that acquire the infection by ingesting fish (second intermediate and/or paratenic host), which in turn become infected by ingesting the third-stage larvae present in freshwater Oligochaeta (intermediate host) (Anderson, 2000). Therefore, the finding of only one third-stage larva of Eutrongylides sp. in a single host, in addition to helminth biology, may signal that the infection was accidentally acquired and that T. dorbigni is an unlikely host for this Nematoda. Occurrence of Neopolystoma sp. and T. achavali at low parasite loads may be related to a number of factors, such as environmental characteristics (for both), presence of a suitable intermediate host (T. achavali), and reproductive characteristics (for both). Such factors may influence the development of free and parasitic life forms (intermediate hosts) jeopardizing the success of the species outside the definitive host (freshwater turtle). Nevertheless, the lack of information on Neopolystoma sp. and T. achavali biology compromises conclusions on the low parasitic indices found in T. dorbigni.

The composition of the helminth assemblage of T. dorbigni in southern Brazil showed a significant relationship between the two sampled anthropogenic environments - urban and rural. The relevance of this relationship includes environmental characteristics (quality and flow of water) of the sites analyzed as an important factor for the parasite Taxa. Both flow and quality of water may have influenced helminth assemblage composition and parasitic loads in the two environments, especially in relation to the intermediate host community for the helminths found in T. dorbigni.

With respect to intermediate host, the quality of water of continental freshwater ecosystems is relevant to the expression of the species that live in it from an abiotic point of view (Gamboa et al., 2008). These species are distributed among various trophic levels, including the different hosts a parasite species may need to complete its life cycle. These hosts, intermediate (primary and/or secondary) or paratenic, may be represented by macroinvertebrates. Heteroxenic cycle parasites such as S. contortus, C. emydidius, F. affinis, D. renale and Telorchis spp. may have their parasitological indices influenced by anthropic impacts, which reflects on the availability of intermediate and/or paratenic hosts of these helminths. These impacts may in turn be either directly or indirectly reflected in the success of intermediate and/or paratenic hosts to withstand the resulting environmental changes. The effect of anthropogenic environmental changes on parasites infracommunities is known, especially in fish species (Lafferty, 1997; Lafferty & Kuris, 1999; Sures, 2008) and such observations and records can be extended to other groups of vertebrate hosts. In the case of T. dorbigni, results suggest that S. contortus and P. rohdei may have their cycles and infection success related to less impacted environments, such as rural. In contrast, species such as D. renale and T. corti, have their cycles and infection success more closely related to impacted environments, such as urban. Thus, S. contortus and P. rohdei seem to be more demanding towards environmental quality.

The presence of third-stage D. renale larvae in freshwater turtles in the urban area of the city of Pelotas seems to be linked to the occurrence of infected domestic dogs (definitive hosts), which eliminate Nematoda eggs in the urine recontaminating aquatic urban environments such as ditches and domestic and rainwater sewage or drainage channels, where intermediate hosts (freshwater oligochaetes) and freshwater turtles coexist. The process of eutrophication caused by the demand for organic matter and other household waste in these aquatic urban environments may have favored an increased oligochaeta population, thus promoting the development of the infective form of D. renale. High densities of oligochaetes are usually found in altered aquatic environments due to an increase in food resources and a decrease in oxygen supply, and the ensuing decrease of predators and/or competitors (Martins et al., 2008). Indirect adverse effects of eutrophication on piscivorous birds (Ardeidae) mortality rates due to an increased infrapopulation of Eustrongylides ignotus (Jägerskiöld, 1909) have been reported by Spalding et al. (1993). These results support the hypothesis that channels waters in the urban area of the city of Pelotas, due to their eutrophication by urban waste and the constant supply of urine of dogs infected by D. renale, contributed the cycle of this Nematoda. Rappeti et al. (2017) diagnosed 81 cases of dioctophymatosis in domestic animals in Pelotas. Mascarenhas & Müller (2015a) addressed the aspects related to eutrophication as well as the role of T. dorbigni in the D. renale cycle, pointing to the difficulty of this new host to contribute to the completion of the life cycle of this parasite in a significant way.

Diet studies may support helminth fauna investigation and vice versa. Studies of food webs suggest that approximately 75% of food chain links involve some sort of parasite (Dobson et al., 2008). Ferguson & Smales (2006), evaluated the helminth assemblage of Emydura macquarii (Gray, 1830) (Chelidae), having identified 11 species (Nematoda, Digenea, Aspidogastrea, Monogenoidea and Amphilinidae); these authors concluded that dietary strategies significantly contributed to the variety of helminth species, once most of these species are transmitted through food webs interactions involving intermediate hosts. Trachemys dorbigni is an opportunistic omnivorous species according to studies conducted in Rio Grande do Sul State, Brazil, by Bujes et al. (2007), Hahn et al. (2014), Mascarenhas & Coimbra (2013) and Silveira et al. (2019). After the collection of helminths of present study, Silveira et al. (2019) analyzed the diet of the specimens and identified several items such as: gastropod molluscs, crustaceans (Cladocera, Decapoda), Blattodea oothecae, dipteran larvae and pupae, ants, filamentous algae. The omnivorous diet of T. dorbigni corroborates the information on the life history of S. contortus, C. emydidius, F. affinis, D. renale and Telorchis spp. (Anderson, 2000; Font & Lotz, 2008). In this context, the helminth assemblage composition and differences in parasite loads of S. contortus, C. emydidius, F. affinis, D. renale and T. corti between individuals from rural and urban environments may be related to the availability of intermediate and/or paratenic hosts, which should be ingested to continue the helminth cycle. Esch et al. (1979), upon analyzing the diversity of intestinal helminth Trachemys scripta (Thunberg in Schoepff, 1792) (Emydidae) in six habitats thermally influenced by a nuclear reactor noted greater diversity as to chemical and physical characteristics in more stable places, suggesting that diversity may result from the complexity of the parasiteʼs life cycle. In order to evaluate diet influence on helminth acquisition, one should also take into account that the diet of freshwater turtles can vary in relation to maturity and gender (Teran et al., 1995; Souza, 2004; Brasil et al., 2011; Hahn et al., 2014).

Another issue that should be considered in helminth studies associated with freshwater organisms refers to water flow influence on helminth infection. Lentic environments are represented by ponds and lakes, which can be classified as polymictic or monomictic according to the mix layer dynamics in the water column, inasmuch as lotic environments (e.g. rivers), have a steady stream of water (Margalef, 1983). It is believed that differences in water flow between rural ponds and urban channels can influence freshwater turtle helminth assemblage. In periods of heavy rain, urban channels in the city of Pelotas have an intense water flow and are characterized as lotic environments, once the rainwater collected is poured into the São Gonçalo Channel. In this context, stands out infections by Monogenoidea, which do not require intermediate hosts to complete their life cycles. Parasites monogenean of fish have been studied so as to assess environmental impact under different approaches such as effluent and heavy metal concentrations and dam building (Dušek et al., 1998; Bayoumy et al., 2008; Madi & Ueta, 2009; Acosta et al., 2013). With regard to the influence of the lentic or lotic environment in the presence of parasites monogenean of fish, Acosta et al. (2013) found a higher prevalence and mean abundance of Steindachnerina insculpta (Fernández-Yépez, 1948) monogeneans in a lentic environment. Similarly, monogenean P. rohdei was found to be significantly more prevalent in rural hosts. Polystomoides species also show peculiar reproductive characteristics as to egg production (Price, 1939). Paul (1938) has reported that Polystomoides oris (Paul, 1938) laid two or three eggs/day and Pichelin (1995) has reported that Polystomoides australiensis (Rohde & Pearson, 1980) laid about six eggs/day. Therefore, it is likely that the water flow in urban area channels, added with the reproductive features of this group as to egg production, hampers the encounter between larvae (oncomiracidia) and hosts, thus playing a negative role on P. rohdei infection success in the freshwater turtles population in that environment. On the other hand, lentic environments such as rural ponds would act positively in P. rohdei colonization of hosts.

Freshwater turtle’s gender implications on helminth’s assemblage of T. dorbigni. In the study the helminth parasite assemblage of T. dorbigni presented a dominant-female host pattern concerning to heteroxenic parasites S. contortus, F. affinis, C. emydidius and T. corti whenever infections were compared between genders either considering the same environment or all hosts. Such gender-dependent differences (or heterogeneities related to gender) detected may be related to two main hypotheses: a) differences in qualitative and quantitative food demands; b) differences neuroendocrine in relation to host’s gender.

With regards to qualitative and quantitative food differences, the likely dominant-female host pattern of T. dorbigni helminth infections could be related to differences in reproductive energy demands (vitellogenesis and development of the amniote egg) as well as to derived sexual dimorphism in larger females. As in this study, Bager et al. (2010), in southern Brazil, have reported that females were greater than males of the T. dorbigni. The diet of some freshwater turtle species may vary qualitatively and quantitatively between males and females, as observed for T. dorbigni (Hahn et al., 2014; Silveira et al., 2019); these authors found significant gender differences, with females having a diet which included a greater diversity of food items than males. Hahn et al. (2014) reported that animal origin items (both invertebrate and vertebrate) accounted for 16.4% of the total food items in females as contrasted to 8.3% in males. As to invertebrate consumption, Hahn et al. (2014) observed that females fed on 16 different groups (Gastropoda, Crustacea, Insecta, Arachnida and Hirudinea), of which crustaceans were the most frequent. On the other hand, males had the diet that comprised of four different food groups belonging to Gastropoda, Insecta and Hirudinea, the most frequent of which were insects. Teran et al. (1995) have suggested that Podocnemis unifilis (Troschel, 1848) (Podocnemididae) females eat more fish and molluscs to meet their calcium needs for the production of eggs.

In this context, the importance of crustaceans and gastropods as intermediate hosts of various groups of helminths, among which Nematoda (e.g. Camallanidae and S. contortus), which use copepod crustaceans (Hedrick, 1935; Anderson, 2000), and Digenea (e.g. Telorchis spp.), which use gastropod molluscs with intermediate hosts (Font & Lotz, 2008) is emphasized.

The parasitic indices of helminth parasites of T. dorbigni may also have been influenced by processes related to neuroendocrine differences between genders. Klein (2004) argues that the male tends to undergo an immunosuppression process both related to testosterone and its derivatives as it matures sexually, and to species with marked reproductive seasonality. On the other hand, Morales-Montor et al. (2004) have pointed out that the female supremacy paradigm in the face of a parasitic infection constraint should be carefully considered, taking into account the heterogeneities of host and parasite species. Additionally, Wirsing et al. (2007) have pointed out that the understanding of parasitic loads (= parasitic indices) relationships should be species-specifically developed in the host-parasite relationship, as research tends to investigate and analyze metacommunities, as discussed by Wirsing et al. (2007). Thus, immune dimorphism meanings can be discussed within their peculiarities. Studies with lizards have demonstrated that males show higher parasitic loads with reference to nematode infections (Sousa et al., 2007; Pereira et al., 2012). As to freshwater turtles, host gender has been little explored in studies of the helminth fauna. Zelmer & Platt (2009), upon analyzing Chelydra serpentina (Linnaeus, 1758) (Chelydridae) infracommunity similarities, produced results suggesting differences in helminth abundance between males and females host. However, these same authors call attention to host’s gender sampling discrepancies (higher for males) and limited themselves to pointing out differences in similarity indices between environments with reference to C. serpentina males only.

Another important immunosuppressive factor which may exacerbate gender’s heterogeneities refers to host-acting pollutants. Different studies have shown that pollutants can affect both host and parasite health (MacKenzie et al., 1995; Lafferty et al., 2004) and, within this context, there is a pollutant-host-parasite feedback along the lifespan of the different species involved. Also, both parasites and pollutants can trigger important hormonal, sexual (=gender-related) and stress changes (Sures, 2008) by triggering a complex neuroendocrine network of homeostatic interaction (Nava-Castro et al., 2011). So, pollutants can exacerbate and feedback heterogeneity influences on T. dorbigni females regarding reproductive physiological pressures.

In short, the results obtained suggest that the gastrintestinal helminths have the a positive association with females, that related to different heterogenic factors of the T. dorbigni, such as derived sexual dimorphism for larger females, probably leading to differences in energy investment between genders (mainly in vitellogenic processes), and resulting in a qualitative and quantitative diet of primary and secondary helminth hosts according to the impact of negative interactions in human environments. However, immunosuppressive factors that may be present in the urban habitat cannot be discarded.

Acknowledgements.

We would like to thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for the permission to capture the freshwater turtles, to Coordenação de Aperfeiçoamento do Pessoal de Nível Superior (CAPES) for the scholarship for CSM and financial support (process number 032/2010). Special thank to Marco Antonio A. Coimbra, Mariana de Moura Mendes and Jéssica Dias Souza for their assistance.

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Publication Dates

• Publication in this collection
  13 Aug 2021
• Date of issue
  2021

History

• Received
  13 Oct 2020
• Accepted
  03 May 2021